Submitted to: Molecular Plant
Publication Type: Peer reviewed journal
Publication Acceptance Date: 1/17/2010
Publication Date: 2/10/2010
Publication URL: hdl.handle.net/10113/46742
Citation: Liu, J., Allan, D.L., Vance, C.P. 2010. Systemic Signaling and Local Sensing of Phosphate in Common Bean: Cross-Talk Between Photosynthate and MicroRNA399. Molecular Plant. 3(2):428-437. Interpretive Summary: Plants require phosphorus (P) for high yields and good seed quality. However, P acquisition by plants is a conundrum. In developed countries like the U.S. there is frequently too much P in the soil and much is lost to runoff causing surface water pollution. While in the developing world P is unavailable due to cost and transport. Improving P acquisition by plants would aid in reducing P fertilizer use in the U.S. and help to efficiently provide currently unavailable P to plants in the developing world. In this study we have evaluated how common bean roots adapt to P-deficiency. Under P-deficiency many plants make a signal comprised of small pieces of genetic material designated miR399. It is thought that miR399 is required for the plant to recognize it is P-deficient. We show here that bean roots can recognize the presence of P in the soil very rapidly (within minutes) and this recognition does not involve miR399. In addition, we show that the formation of miR399 requires sugar in the form of photosynthate. If photosynthesis is blocked or the transport of photosynthate sugars is blocked, then miR399 is either not produced or drastically reduced. Our results indicate that P-deficiency signaling in bean involves crosstalk between miR399 and sugars. The data also suggest that some aspects of P-deficiency signaling are independent of miR399 and these aspects occur very rapidly. Our findings support the hypothesis that there are multiple P-deficiency signaling pathways in plants and improvement of P-use efficiency will require combined modification of miR399 and plant sugars.
Technical Abstract: Shoot-to-root communication is crucial for plant adaptation to phosphorus (P) deficiency. Both sugars and miRNAs have been implicated as potential signal molecules transported through phloem from shoot to root for the regulation of gene expression and Pi uptake in the root. By studying the expression patterns of both a serine/threonine phosphatase gene (PvHAD1) and microRNA399 (miR399) in common bean (Phaseolus vulgaris L.), we provide evidence for the interaction between light, phloem transport, and miR399 in the systemic regulation of gene expression under P deficiency. Especially, miR399 expression in both the shoot and the root requires photosynthetic carbon assimilation during the onset of P deficiency. In contrast to systemic signaling, local sensing was the primary causal factor for rapid down regulation of PvHAD1 by Pi prior to the reduction of miR399 transcript level in P-deficient roots. Furthermore, this initial response to Pi in P-deficient roots was also mimicked by the Pi analog, phosphonate (Phi). Our current findings suggest that plants have developed a highly coordinated dual regulatory pathway, i.e. long-distance signaling of P-deficiency from shoot to root vs. local sensing of Pi in the root.